Models of parent-offspring conflict. II. Promiscuity

The population genetics of Trivers (1974) concept of parent-offspring is examined for species in which the effects of the conflict are felt by future half-sibs, as in promiscuous mating systems in which the male shows no parental care. Whether or not a rare conflictor gene will spread in a non-conflictor population depends on f(m) greater than (m + 1)/(0.5m + 1.5) for a dominant gene, and on f(m) greater than 1/4(7 + 3) for a recessive gene; f(m) is the fitness gained by a conflictor relative to a non-conflictor offspring [f(m) greater than 1], and m is the amount of parental investment taken by a conflictor relative to m = 1 for a non-conflictor. The ESS value for conflict (mo) in promiscuous species with zero male parental care has mo = f(mo)/4[df(mo)/dmo]. However, where the male maintains the same harem for several breeding seasons, or where there is promiscuity but both sexes contribute equally to parental care, conditions for conflict are equivalent to monogamy.     

Models of parent-offspring conflict. III. Intra-brood conflict

A genetic model of parent-offspring conflict is developed for the situation where conflictors cause the parent to redirect resources from contemporaneous siblings to themselves, by increased solicitation. It is shown that there is no restriction on the spread of genes causing such conflict if there is no direct cost associated with it. We examine the effect of imposing on the conflictors a cost of the extra solicitation when the cost is felt (a) by the individual conflictor only, and (b) by all members of the brood equally. It is shown that the Evolutionarily Stable Strategies for the two situations allow a greater degree of solicitation when its cost is borne by the whole brood. Multipaternity of broods also increases the degree of conflict.     

Models of parent-offspring conflict. IV. Suppression: Evolutionary retaliation by the parent

We have earlier analysed ESSs for the amount of parental investment (PI) that offspring are expected to solicit from their parents, given that parents acquiesce to offspring demands. The present paper considers evolutionary retaliation by the parent for species where only one parent provides PI. Two genetic loci are envisaged: one (the ‘conflictor’ locus) determines the extent of offspring solicitation; the other (the ‘suppressor’ locus) determines how parents retaliate. Solicitation is assumed to carry a cost which may affect a particular offspring uniquely if time and energy are the major costs, or may affect all offspring in a brood equally if the main cost is predation risk. Two kinds of parental retaliation are possible. Parents may supply PI in proportion to offspring demands, or may ignore solicitation altogether and give a fixed PI. Analytical models of conflict in which the parent supplies PI in proportion to solicitation yield pure ESSs with PI at a compromise level between parent and offspring interests. These are termed ‘pro rata’ ESSs. Where solicitation costs are high, an ‘offspring wins’ ESS (offspring get all they ‘want’) is possible especially for forms of conflict that affect future sibs, and a ‘parent wins’ ESS (parent supplies its optimum) is possible especially for conflict that affects contemporary sibs. When parental retaliation takes the form of ignoring offspring solicitation, this can lead to a ‘parent wins’ ESS if costs of ignoring solicitation are negligible, but where parental insensitivity carries costs, the result is an unresolvable evolutionary chase with cycling frequencies of alleles coding for parent and offspring strategies. ‘Pro rata’ ESSs cannot be invaded by ‘ignore solicitation’ mutants but ‘pro rata’ mutants can often invade at certain stages in ‘ignore solicitation’ limit cycles. We therefore conclude that the probable evolutionary end product for most species will be the ‘pro rata’ ESS in which the parent supplies more PI than would be optimal in the absence of conflict, but less PI than would be an ESS for the offspring in the absence of parental retaliation. Such ESSs will be characterized by solicitation costs; offspring will ‘ask’ for more PI than they get. In nature, under similar conditions, highest conflict will occur when both parents sustain equally the effects of conflict, or when conflict affects contemporary rather than future sibs.     

Models of parent-offspring conflict. V. Effects of the behaviour of the two parents

In the absence of any parent-offspring conflict, the total parental investment per offspring should be less when two parents collaborate in caring for the offspring than when only one parent invests. This does not necessarily mean that offspring fare less well when both parents invest. The ‘ideal’ amount of parental investment for an offspring to take is always greater than is ‘ideal’ for the parent to allocate (Trivers 1974). The offspring's optimum is higher if the offspring's action affects the reproductive success of only one parent and lower if both parents are affected (e.g. two-parent investment, or lifelong monogamy). The difference between the parental optimum and the offspring optimum depends on the mating system and on the form of conflict (between successive broods, or within broods), and prescribes a ‘conflict range’. The extent of conflict cannot be deduced solely from a knowledge of the average relatedness between siblings. The conflict is likely to be resolved by an ESS in which intermediate (compromise) levels of investment are paid out to offspring, which nevertheless continue to make costly demands for yet more investment. The degree of conflict can be measured by the extent to which offspring subject their parents to aggressive demands for extra investment, and is likely to be greater when two parents collaborate equally over investment than when only one parent invests. When only one parent invests, conflict is higher if sibling-competition is between siblings in the same broods (intra-brood) than when it is between progeny in successive broods (inter-brood). However, the reverse will tend to be the case when both parents invest equally.     

Shared and unshared parental investment,parent-offspring conflict and brood size

Taking as our starting point Trivers' (1974) account of parent-offspring conflict, we develop models of the influence of brood size on the optimal level of parental investment (PI) in the whole brood for parent and offspring, and on the magnitude of conflict between them. A modification of Trivers' model is proposed. In general, the benefit of an act of PI to an offspring in a brood of size N is (N+1)/N times the benefit to its parent. Therefore as brood size increases, offspring benefit approaches parental benefit, and this is because an increasing proportion of the offspring's benefit is being gained through siblings, to which offspring and parent are equally related. A distinction is drawn between ‘shared’ and ‘unshared’ types of PI. When PI is shared the total benefit accruing is not directly gained by all offspring but is shared amongst them (e.g. food brought to the young). In contrast, unshared PI can simultaneously benefit some or all of the brood (e.g. types of anti-predator defence). For shared investment, PI and conflict are predicted to increase with brood size. Two models of unshared anti-predator defence are described. If the predator characteristically takes the whole brood when it strikes (e.g. altricial nestlings) PI is predicted to increase and conflict decline with brood size, although this effect is inhibited or even reversed for high risk defence tactics because of the higher cost to larger broods if the parent dies. When the predator takes a single offspring (e.g. precocial birds) the parent's optimum PI is independent of brood size, the offspring's optimum PI declines in larger broods and conflict again declines with brood size. The parent is commonly expected to win the conflict over anti-predator care. Predictions concerning PI levels gain support from existing data, largely for birds, but evaluation of those for conflict must await the collection of new data. The distinction between shared and unshared investment is applicable to altruistic behaviour in general.     

Parent-offspring conflict over the transmission of culture

Trivers (Am. Zoologist 14:249, 1974) introduced concept of parent-offspring conflict and discussed juvenile rebellion against parental values as a possible example of conflict behavior. The study of parent-offspring conflict over the transmission of culture has, however, remained relatively unexplored, despite the importance of enculturation and social learning by the young in all human societies and in a large number of animal societies. In this report I study the effects of interlinked historical change in genetic and cultural information (gene-culture coevolution) on the cost-benefit structure of parent- offspring conflict as expressed in two basic models of the process: the original microeconomic model of Trivers (1974), and a one-locus, population-genetic analogue reported by Stamps et al. (Behav. Ecol. Sociobiol. 3:369, 1978). The Trivers model incorporates fitness based on the reproductive success of individuals, whereas the Stamps model utilizes the concept of the relative fitness of alleles. Previous studies have suggested that during gene-culture coevolution, innate constraints on mental development are likely to arise, which make offspring more likely to learn fitness-enhancing cultural information, rather than information that is more nearly neutral or deleterious to their reproductive success. These proposed constraints have been termed epigenetic rules. When considered in the context of parent-offspring relationships as modeled by the formulations of Trivers and Stamps et al., epigenetic rules are found to reduce the potential for parent-offspring conflict over the transmission of culture. Further analysis of the one-locus model indicates that alleles prescribing the epigenetic rules can render selfish acquisition of culture too costly for an offspring and thereby remove the underlying genes from the population. The predictions obtained from the theoretical analysis are compared to the existing information on enculturation in human societies, and found to be in general accord with the available data.     

An asymmetric parental investment conflict with continuous strategy sets

In the parental investment conflict each of the sexes decides how much to invest in its brood, where its decision influences both sexes' fitness. In nature, each species is usually characterized by a common parental care pattern, male-only care, female-only care or biparental care. A possible way for understanding the factors that have led each species to adopt its unique parental care pattern is to analyse a male's and a female's decision process using a game-theoretical model. This paper suggests a two-stage game-theoretical model with two types of players, male and female. During the game each parent makes three decisions. The interval between the beginning of the game, i.e. after mating and having offspring, and the moment a parent starts to care for them is a random variable. Thus, in the first stage a parent chooses the cumulative probability distribution of this interval, and its amount of parental care. In the second stage the other parent chooses its probability for cooperation. It is assumed that as long as parental care is not provided the offspring are at risk, and that parental caring accrues a different cost for each sex. We compute the Evolutionary Stable Strategies (ESS) under payoff-relevant asymmetry, and show that uniparental and biparental care are possible ESS. We also characterize cases where the sex having the lower cost "forces" the sex having the higher cost to care and vice versa.     

Parent-Offspring Conflict

When parent-offspring relations in sexually reproducing speciesare viewed from the standpoint of the offspring as well as theparent, conflict is seen to be an expected feature of such relations.In particular, parent and offspring are expected to disagreeover how long the period of parental investment should last,over the amount of parental investment that should be given,and over the altruistic and egoistic tendencies of the offspringas these tendencies affect other relatives. In addition, undercertain conditions parents and offspring are expected to disagreeover the preferred sex of the potential offspring. In general,parent-offspring conflict is expected to increase during theperiod of parental care, and offspring are expected to employpsychological weapons in order to compete with their parents.Detailed data on mother-offspring relations in mammals are consistentwith the arguments presented. Conflict in some species, includingthe human species, is expected to extend to the adult reproductiverole of the offspring: under certain conditions parents areexpected to attempt to mold an offspring, against its betterinterests, into a permanent nonreproductive.     

Packaging of offspring by nests of the ant,Leptothorax longispinosus: parent-offspring conflict and queen-worker conflict

Models of the packaging of offspring predict that parental fitness is maximized by following a set of rules, including the rule to invest the minimal amount in each offspring. Offspring can maximize their fitness by demanding more resources than the parent is selected to give, leading to parent-offspring conflict over packaging. Social insect nests may also experience queen-worker conflict over packaging. Experiments were conducted, using two populations of the ant Leptothorax longispinosus, in order to determine the role of both parent-offspring conflict and queen-worker conflict in packaging. Parent-offspring conflict over packaging was detected towards males and workers, but not to females. This may be because both parental and offspring fitness are maximized by investing as much in possible in females so both parties benefit by cooperating over packaging of females. Queen-worker conflict over packaging was detected for females, males, and workers. The direction taken by the queen-worker conflict is best explained by asymmetries in genetic relatedness among nestmates.     

Parental supply and offspring demand amongst Karo Batak mothers and children

The resolution of parent-offspring conflict (POC) might sway in favour of the offspring if the parent relies on offspring-supplied information about need. Here, three hypotheses from a resolution model of POC were tested using data on sickness histories and mother-infant interactions from 24 Karo Batak women and their young children from two rural villages in North Sumatra, Indonesia. First, as predicted, offspring with greater need (measured as age and propensity to illness) tended to fuss more often. Second, as expected, observed fussiness predicted the number of suckling occurrences observed during sampling periods. Third, contrary to the prediction, the duration of fussing observed after breast-feeding occurrences was longer than the duration of the breast-feeding occurrences themselves. Parental decisions were made based on offspring-supplied information about need, but offspring failed to garner resources in excess of the parental optimum. This suggests that a POC interpretation is unnecessary to account for these results.     

The risks of parenthood II. Parent-offspring conflict

Summary Previous work has demonstrated the value of dynamic programming models for the analysis of parental decision making. In the present paper we extend this approach to analyse conflicts between parents and their offspring, and develop a dynamic ESS model of feeding and fledging of nestling birds. In order to simplify the formulation and solution of the dynamic ESS model, we adopt an assumption of alternating decisions: in each time period the parent first decides whether to continue provisioning the nestling, after which the nestling decides whether to leave the nest. The model takes into account numerous tradeoffs involved in parent-offspring decisions, including differential growth and mortality rates for offspring in and out of the nest, risk of fledging, relation between long-term survival and post-breeding mass of offspring, and parental mortality risk associated with provisioning of offspring. Depending on assumed parameter values, the model is capable of predicting a wide range of feeding-fledging behaviour. The model is applied specifically to the juvenile life history of dovekies (Alle alle), and provides a behavioural explanation for the phenomenon of pre-fledging mass recession in this species.     

The coadaptation of parental supply and offspring demand

The evolution of parent-offspring interactions for the provisioning of care is usually explained as the phenotypic outcome of resolved conflicting selection pressures. However, parental care and offspring solicitation are expected to have complex patterns of inheritance. Here we present a quantitative genetic model of parent-offspring interactions that allows us to investigate the evolutionary maintenance of a state of resolved conflict. We show that offspring solicitation and parental provisioning are expected to become genetically correlated through coadaptation and that their genetic architecture is dictated by an interaction between patterns of selection and the proximate mechanisms regulating supply and demand. When selection is predominately on offspring solicitation, our model suggests that the genetic correlations between provisioning and solicitation are usually positive if provisioning reduces solicitation. Conversely, when selection is predominately on parental provisioning, the correlations are mostly negative as long as parents show a positive response to offspring demand. Empirical estimates of the genetic architecture of traits involved in family interactions fit these predictions. Our model demonstrates how the evolutionary maintenance of parent-offspring interactions can result in variable patterns of coadaptation, and it provides an explanation for the diversity of family interactions within and among species.     

How costly is the honest signaling of need?

ESS models of biological signaling have shown that costly signals can provide honest information. In the context of parent-offspring conflict over the allocation of resources by parents to their young, the theory explains costly offspring solicitation behavior as an accurate signal of offspring need to parents who cannot assess offspring condition directly. In this paper, we provide a simple but general characterization of the honest signaling of need in models of parent-offspring conflict: the offspring's signaling cost is proportional to the parent's fitness loss from satisfying the offspring's resource requirement. The factor of proportionality is given by a measure of the extent of parent-offspring conflict that depends only on coefficients of relatedness. These results hold for interbrood conflict with uniparental investment even if the relationship between offspring condition and resource requirement is not monotonic, and extend to cases of biparental care, uncertainty concerning the parent's condition, and intra-brood conflict. Copyright 1999 Academic Press.     

Evolution of polyembryony: Consequences to the fitness of mother and offspring

Polyembryony, referring here to situations where a nucellar embryo is formed along with the zygotic embryo, has different consequences for the fitness of the maternal parent and offspring. We have developed genetic and inclusive fitness models to derive the conditions that permit the evolution of polyembryony under maternal and offspring control. We have also derived expressions for the optimal allocation (evolutionarily stable strategy, ESS) of resources between zygotic and nucellar embryos. It is seen that (i) Polyembryony can evolve more easily under maternal control than under that of either the offspring or the ‘selfish’ endosperm. Under maternal regulation, evolution of polyembryony can occur for any clutch size. Under offspring control polyembryony is more likely to evolve for high clutch sizes, and is unlikely for low clutch sizes (<3). This conflict between mother and offspring decreases with increase in clutch size and favours the evolution of polyembryony at high clutch sizes, (ii) Polyembryony can evolve for values of “x” (the power of the function relating fitness to seed resource) greater than 0.5758; the possibility of its occurrence increases with “x”, indicating that a more efficient conversion of resource into fitness favours polyembryony. (iii) Under both maternal parent and offspring control, the evolution of polyembryony becomes increasingly unlikely as the level of inbreeding increases, (iv) The proportion of resources allocated to the nucellar embryo at ESS is always higher than that which maximizes the rate of spread of the allele against a non-polyembryonic allele.     

Response to vocal music in Angelman syndrome contrasts with Prader-Willi syndrome

Parent-offspring conflict—conflict over resource distribution within families due to differences in genetic relatedness—is the biological foundation for many psychological phenomena. In genomic imprinting disorders, parent-specific genetic expression is altered, causing imbalances in behaviors influenced by parental investment. We use this natural experiment to test the theory that parent-offspring conflict contributed to the evolution of vocal music by moderating infant demands for parental attention. Individuals with Prader-Willi syndrome, a genomic imprinting disorder resulting from increased relative maternal genetic contribution, show enhanced relaxation responses to song, consistent with reduced demand for parental investment (Mehr, Kotler, Howard, Haig, & Krasnow, 2017, Psychological Science). We report the necessary complementary pattern here: individuals with Angelman syndrome, a genomic imprinting disorder resulting from increased relative paternal genetic contribution, demonstrate a relatively reduced relaxation response to song, suggesting increased demand for parental attention. These results support the extension of genetic conflict theories to psychological resources like parental attention.     

Heterosis in hybrids within and between yeast species

The performance of hybrids relative to their parents is an important factor in speciation research. We measured the growth of 46 Saccharomyces yeast F1 interspecific and intraspecific hybrids, relative to the growth of each of their parents, in pairwise competition assays. We found that the growth of a hybrid relative to the average of its parents, a measure of mid‐parent heterosis, correlated with the difference in parental growth relative to their hybrid, a measure of phenotypic divergence, which is consistent with simple complementation of low fitness alleles in one parent by high fitness alleles in the other. Interspecific hybrids showed stronger heterosis than intraspecific hybrids. To manipulate parental phenotypic divergence independently of genotype, we also measured the competitive growth of a single interspecific hybrid relative to its parents in 12 different environments. In these assays, we not only identified a strong relationship between parental phenotypic divergence and mid‐parent heterosis as before, but, more tentatively, a weak relationship between phenotypic divergence and best‐parent heterosis, suggesting that complementation of deleterious mutations was not the sole cause of interspecific heterosis. Our results show that mating between different species can be beneficial, and demonstrate that competition assays between parents and offspring are a useful way to study the evolutionary consequences of hybridization.     

Marker-based prediction of the parental genome contribution to inbred lines derived from biparental crosses

Molecular markers can be employed to predict the parental genome contribution to inbred lines. The proportion alpha of alleles originating from parent P1 at markers polymorphic between the parental lines P1 and P2 is commonly used as a predictor for the genome contribution of parent P1 to an offspring line. Our objectives were to develop a new marker-based predictor xi for the parental genome contribution, which takes into account not only the alleles at marker loci but also their map distance, and to compare the prediction precision of xi with that of alternative methods. We derived formulas for xi for inbreds derived from biparental crosses (F1 and backcrosses) with the single-seed descent or double-haploid method and presented an extension xi* possessing statistical optimum properties. In a simulation study, alpha showed a systematic overestimation of large parental genome contribution that was not observed for xi. The mean squared prediction error of xi was at least 50% smaller than that of alpha for linkage maps with unequal distances between adjacent markers. A data set from a study on plant variety protection in maize was used to illustrate the application of xi. We conclude that xi provides substantially greater prediction precision than the commonly used predictor alpha in a broad range of applications in genetics and breeding.     

Co-operation and defection: playing the field and the ESS

If food is patchily dispersed, food clumps being very rich, but rare and hard to find, each individual in a foraging flock then faces an evident dilemma: whether to co-operate and participate in the search, thus enhancing the rate by which rich patches are discovered, or to defect and let others do the searching, thus avoiding any possible expenditures and risks involved in the search (but enjoying the abundant resources once a rich patch is discovered). This conflict (and its possible solution) is treated as an example in the analysis of the synergistic n-player game presented in this paper. After deriving conditions for the existence of a mixed ESS in such games, the evolutionary stability of the mixed strategy against invasions by pure strategists, in particular against invasions by recognizable defectors, is analyzed. Whereas in any "degenerating" mixed-strategy model a recognizable defector can invade and spread, a "non-degenerating" model can sometimes yield a mixed ESS which is immune to such invasions.     

Parent-offspring conflict and co-adaptation: behavioural ecology meets quantitative genetics

The evolution of the complex and dynamic behavioural interactions between caring parents and their dependent offspring is a major area of research in behavioural ecology and quantitative genetics. While behavioural ecologists examine the evolution of interactions between parents and offspring in the light of parent-offspring conflict and its resolution, quantitative geneticists explore the evolution of such interactions in the light of parent-offspring co-adaptation due to combined effects of parental and offspring behaviours on fitness. To date, there is little interaction or integration between these two fields. Here, we first review the merits and limitations of each of these two approaches and show that they provide important complementary insights into the evolution of strategies for offspring begging and parental resource provisioning. We then outline how central ideas from behavioural ecology and quantitative genetics can be combined within a framework based on the concept of behavioural reaction norms, which provides a common basis for behavioural ecologists and quantitative geneticists to study the evolution of parent-offspring interactions. Finally, we discuss how the behavioural reaction norm approach can be used to advance our understanding of parent-offspring conflict by combining information about the genetic basis of traits from quantitative genetics with key insights regarding the adaptive function and dynamic nature of parental and offspring behaviours from behavioural ecology.     

PROXIMATE AND ULTIMATE CONTROLS ON LIFE-HISTORY VARIATION: THE EVOLUTION OF LITTER SIZE IN WHITE-FOOTED MICE (PEROMYSCUS LEUCOPUS)

Recruitment of litter-mates of nest-box-inhabiting white-footed mice was monitored to study the evolution of litter size. The frequency distribution of litter sizes was nonsymmetrical, and the most frequent litter size was less than the optimum. This was not the result of differential parental survival, which was independent of litter size produced. Recruitment remained constant or increased slightly to a peak in litters of five young, and then dropped precipitously for larger litters. The single optimum litter size of five did not appear to have any physiological correlates. Instead, the equally low probability of successful recruitment of any young from any given litter may have given rise to a bet-hedging strategy of frequent iterated reproductions. A theoretical analysis of optimal parental investment in offspring was initiated under the assumption that optimal brood size represents a maximization of differences between age-specific costs and benefits of reproduction, both of which should be measured in constant currency of inclusive fitness. In the past, benefit has been measured by current fecundity, and cost by residual reproductive value. However, reproductive value is an appropriate estimate of inclusive fitness only for organisms in which parental investment has little effect on the subsequent survival of offspring to reproductive age. Reproductive value weighted by offspring survival and devalued by the degree of genetic relatedness defines a new currency, replacement value, which is more appropriate for evaluating the costs and benefits of parent-offspring conflict over parental investment in current as opposed to future young. Total parent-offspring conflict intensifies with increases in current brood size. For species with severe reproductive constraints, such as post-partum estrus in white-footed mice, such conflict may force parents to curtail investment in current offspring at or near parturition of subsequent litters, even if that means reducing the survival of current young.